Kusmarinah Bramono: Chronic Recurrent Dermatophytosis in the Tropics: Studies on Tinea Imbricata in Indonesia

Korean J Med Mycol 17(1), 2012 Invited Lecture

Chronic Recurrent Dermatophytosis in the Tropics:

Studies on Tinea Imbricata in Indonesia
Kusmarinah Bramono
Department of Dermato-Venereology, Faculty of Medicine, University of Indonesia, Jakarta
= Abstract =

Dermatophytosis is one of the major public health problems in tropical countries, especially the
chronic recurrent type. Tinea imbricata (TI), a dermatophytosis caused by Trichophyton concentricum
(TC), is endemic in several remote and isolated areas in Indonesia. This dermatophytosis is unique due
to its predominant genetic predisposition, which leads to chronic recurrent conditions among the affected.
Moreover, hot and humid climate, low socio-economic conditions, lack of hygiene, inadequate treatment
due to difficult access to health care facilities, and persistent source of re-infections, are among other
factors that maintain the chronic-recurrent state. Studies on TI in Indonesia have been done since the 1960s,
encompassing the epidemiology, clinical features, and efficacy of antifungal treatment. Griseofulvin is
still the mainstay treatment, but relapse rates are high. The latest effort in reducing relapse includes the
training of healthcare providers and provision of fungal disinfectant for clothing and bedding to patients
in West Papua in addition to standard treatment. Higher cure rate was achieved at the end of treatment
and the four-month follow-up in comparison to previous studies. Parallel studies on the same patient
populations showed that: 1. clothing and bedding were fomites and potential sources of re-infections; 2.
sodium hypochlorite worked well as a fungal disinfectant, followed by anionic detergent and pine oil
containing cleaner; 3. terbinafine was the most effective antifungal agent for TC in vitro, followed by
griseofulvin; itraconazole, and fluconazole were less effective. In conclusion, to eradicate TI in endemic
areas, appropriate and affordable antifungal treatment, concurrent with health education and efforts to
identify and eradicate the source of re-infections are very important.
[Korean J Med Mycol 2012; 17(1): 1-7]
Key Words: Tinea imbricata, Indonesia

high humidity are ideal environment for fungal

INTRODUCTION
Dermatophytosis is still an important public
health problem in the world, especially in tropical
countries where yearlong warm temperature and
Received: September 3, 2011
growth. This disorder is not fatal, but the in-
tractable pruritus and cosmetic disfigurement that
affect the patients can decrease their quality of life
and productivity. The chronic recurrence condition
will create an economic burden, and the repeated

Corresponding author: Kusmarinah Bramono, jl. Bambu Kuning # 15 Jakarta, 12560 Indonesia.
Tel: +62-21-7812677, Fax: +62-816-808336, e-mail: kbramono@yahoo.com
*
The author is thankful to the local government and health authorities of Raja Ampat, the co-workers, and to the University of Indonesia
for the Community Development Grant 2009 no. 2897/H2.R12/PPM.01.
The complete results of the studies will be published separately.

-1-
Kor J Med Mycol 17(1), 2012
and long-term treatment will increase the risk of
antifungal resistance. Recurrences could be related
to inadequate treatment, difficulties in eliminating
the predisposing factors, and unnoticed source of
re-infection.
One type of chronic recurrent dermatophytosis
is tinea imbricata (TI), which has many local
synonyms such as kaskado in Papua, kihis in
Central Kalimantan, chimbere in Bolivia, and le
pita in Tokelau island. TI is endemic in several
remote and isolated tropical areas in South Pacific,
South-East Asia, Central and South America, and
Mexico1,2. In Indonesia, the endemic foci are
located in Sulawesi, Papua, Kalimantan, and some
of the islands in the middle part of Eastern
Indonesia3.
This dermatophytosis is caused by Trichophyton
concentricum (TC), a slow growing anthropophilic
dermatophyte, that appears to be population-group
specific, as it is found in particular races, but not
easily transmitted to other races. It affects the skin
and scalp, but never on the hair. The nail is some-
times affected. Clinically, it is characterized by
multiple scaly papulosquamous plaques arranged
in concentric rings, with the free edges of the scales
facing the center. There is slight or no erythema.
Early lesions are usually very pruritic, but it may be
absent in the chronic stage. In some cases, clinical
pattern variations can be found due to scratching or
coexistence of other skin diseases. The diagnosis
of TI is mostly based on clinical examination and
direct mycological examination. Fungal culture is
needed when the characteristic concentric rings
are not present2,4.
During the last three decades, several studies on
TI had been done in Indonesia. Several aspects of
TI that can be obtained from those studies, e.g.
epidemiology, clinical patterns, and responses to
treatment with antifungal agents will be discussed
in this manuscript with brief remarks on the related
studies outside of Indonesia. The recent study on
-2-
TI treatment that was conducted in West Papua
with simultaneous studies on the detection of
fomites, effort to eliminate viable TC with dis-
infectants, and sensitivity of TC against antifungal
agents will also be described.
Epidemiology
Indonesia is a vast equatorial archipelago of
around 17,000 islands, with 5 largest islands of
Sumatra, Java, Kalimantan (Indonesian Borneo),
Sulawesi, and the Indonesian part of New Guinea
(known as Papua or Irian Jaya). Based on data from
the 1970s cited by Widyanto5, TI was still endemic
in all the 5 big islands, including the most devel-
oped island Java. The prevalence in Mauk village,
West Java, was very low 7.3/10,000 population
(0.07%). The prevalence in remote areas outside
Java was believed to be much higher, but the
accurate number was not available. However, based
on the prevalence number of 18% in remote area in
New Guinea6 and 9.1% in remote area in Malaya7,
the prevalence in the other islands in Indonesia
must be more or less the same. In Java, TI was
mostly found in the coastal area5,8.
A follow-up study in the 1980s at the same
village of Mauk5 showed a bit lower prevalence of
0.04% (4.3/10,000), with a male to female ratio of
1:1. The youngest was 9-years old and the oldest
was 70 years old, with peak incidence between
40~49 years old. The average duration of the
disease was 17.3 years, ranging from 7.2~27.5
years. In this study, a trichophytin intradermal test
revealed that 97% patients showed no response of
delayed hypersensitivity, indicating decreased cel-
lular immunity. A similar result was also reported
by Hay in his survey in Papua New Guinea9.
In the 1990s, a survey on TI was conducted by
Budimulya in 23 villages located at Central
Kalimantan10. The results revealed average preva-
lence of 2.83%, ranging from 0.06~20.14%. Vil-
 Kusmarinah Bramono: Chronic Recurrent Dermatophytosis in the Tropics: Studies on Tinea Imbricata in Indonesia

Fig. 1. The classic concentric imbricated rings.

Fig. 2. The lamellar pattern with large coarse scales.

lages with low prevalence were located close to
the big cities. The youngest age affected was 6
months old, and the oldest was 70 years old, with
peak incidence between 25~44 years old. This
survey also showed that male and female were
equally affected. They were from low socioeco-
nomic status with low education level and poor
personal and environmental hygiene. A genetic
study in concomitant with the survey confirmed
that susceptibility to TI was inherited through the
autosomal recessive trait, which was already shown
in previous studies11,12.
All of these studies indicated that TI occurs in Fig. 3. The hypochromic pattern which still show
all age group in a chronic manner, which can begin active border.

at a very young age, with no gender predominance.

Despite the persistent high prevalence number
in the endemic foci in Kalimantan and Papua since
the 1990s, the endemic foci in Java is no longer
existent10. Java is currently the most populous
island with mixed ethnicity, and compared to the
other islands it is the most developed in terms of
socioeconomic condition, healthcare facilities, and
transportation. It is possible that those conditions
that are found in Java attributed to the decline of
TI incidence.

-3-
Kor J Med Mycol 17(1), 2012
Clinical patterns
Widyanto5 reported only 20% of his cases suf-
fered from pruritus in Mauk, West Java. He also
revealed that more than 50% of the cases had
widespread lesions on the whole body, with some
involving the scalp and nail. Among the cases with
localized lesions, 80% had characteristic concentric
features; but in cases with widespread lesions, all
of them were ichthyosiformis with no concentric
rings.
Budimulya10 reported that 67% of his cases in
Central Kalimantan had more than 50% skin in-
volvement, while about 17.5% was universally
affected. Unlike the findings by Widyanto, all of
the cases had specific concentric lesion configu-
rations.
Based on the clinical features variation, Hay et
al.13 distinguished 7 different patterns from a study
in Goodenough island, Papua New Guinea in 1984:
concentric, lamellar, lichenified, plaque-like, annular,
palmar/plantar, and onychomycosis. They also
found that hypopigmentation was the prominent
feature. In 2004, Bonifaz et al.1 added 2 more pat-
terns to the list: seborrheic-like and hypochromic/
hyperchromic. It is speculated that the skin clinical
variations are related to chronic scratching.
The study in Raja Ampat found that out of 47
cases, 6 (12.8%) had lesions on the whole body
and 3 (6.4%) with onychomycosis. Pruritus was
present in 89% of the cases. The clinical features
varied, comprising of all proposed by Bonifaz, with
a trend that each village had a particular predomi-
nant feature. It is yet to be investigated whether
the clinical feature variant is only due to chronic
scratching, or also due to different strain of TC or
other patient's habit.
The diagnostic confirmation of TI with direct
fungal examination and culture are necessary since
several reports indicated that concentric rings
-4-
mimicking TI could be present in other skin
diseases14~17. Furthermore, the characteristic feature
is not always present in TI. However, the remote
location of the endemic area makes culture
impractical. The delayed culture examination and
the slow-growing nature of TC, which is easily
contaminated, resulted in low success rate of
isolation as reported by Pihet et al. (33%)18 and
Wingfield et al. (61%)19. Specimen pre-treatment
with 70% alcohol as suggested by Budimulja et
al.5 produced better success rate, as was also shown
by our Raja Ampat Study with 93.6% success rate.
Responses to antifungal treatment
Almost all the TI studies in Indonesia were
associated with antifungal treatment assessment.
In 1965, Halde and Ong8 used various dosage
schedules of griseofulvin on hospitalized cases in
West Java. Eighty eight percent of the cases re-
sponded well to the treatment, but relapse occurred
in 59% of the cases within 3-4-month follow-up.
In 1988, a study in Sulawesi evaluated keto-
conazole at 200 mg/day on 23 cases20. Only 3 out
of the 23 cases showed clinical clearance, but all
of them still showed positive KOH examination.
An open study on griseofulvin 250~500 mg/
day versus terbinafine 250 mg/day for four weeks
was conducted in Central Kalimantan in 199221.
The result was 47.8% and 90% clinical cure and
86.7% and 43.5% mycological cure, respectively
for griseofulvin and terbinafine. Drop-out in the
griseofulvin group was 38%, but none in the
terbinafine group. Relapse rate two weeks later
was 22% in griseofulvin, none in terbinafine. In
1993 the same investigators22 evaluated terbina-
fine at 250 mg/day versus itraconazole at 100 mg/
day for four weeks, and showed 100% clinico-
mycological cure rate in the terbinafine group
versus 88.6% in the itraconazole group. Relapse
rates three months later were 16.2 and 75% for
 Kusmarinah Bramono: Chronic Recurrent Dermatophytosis in the Tropics: Studies on Tinea Imbricata in Indonesia
terbinafine and itraconazole groups respectively.
Drop-out rate was as high as 22.5%.
In 2004, Wingfield et al. compared19 four weeks
terbinafine at 250 mg/day, or griseofulvin 2
500 mg/day, or fluconazole 200 mg/week, and one
week itraconazole 2 200 mg/day for TI patients
in Southern Papua. Drop-outs of 31.4% were
observed. The clinical cure rates were 98%, 80%,
33%, and 8% respectively for the treatments regi-
ments above among the returned cases. Itraconazole
showed the highest relapse rate at follow-up.
Our last study in Raja Ampat islands used a
different approach. To empower the locals to assist
TI treatment program, health education and training
on the detection and management of TI were
conducted for the local healthcare providers (local
doctors, midwives, and nurses) and volunteers.
They were then involved in TI surveillance and
treatment program and case follow-up in their
community. Among a total of 47 cases eligible for
systemic antifungal treatment, griseofulvin 2
500 mg/day for six weeks was given for 28 cases
with an adjusted dose for children. For 11 cases
with a history of unresponsiveness to griseofulvin
or with onychomycosis, terbinafine 250 mg/day
for four weeks (for skin involvement) and three
months (for onychomycosis) were provided. All
patients were given sodium hypochlorite solution
and pine oil containing cleaner to clean their
clothing and bedding in addition to their own daily
used detergents. The healthcare volunteers were
assigned to monitor the treatment and hygiene
compliance. The results which were recorded with
the help of the local healthcare providers showed
89.3% clinical cure rate in griseofulvin group at
the end of treatment and 78.5% at four-month
follow-ups. In the terbinafine group, 100% clinical
cure rate was seen on both observations. There
were 14.6% drop-outs with known reasons, such
as allergic reaction or incompliance. These results
indicated that the involvement of the local health-
-5-
care providers and healthcare volunteers in the TI
controls helped to reduce the drop-out's number.
The higher total dose of griseofulvin might have
contributed to the higher cure rates and lower
relapses.
Fomites and disinfectants in
Trichophyton concentricum
Relapses in dermatophytosis can be due to an
inadequate treatment or inadequate cellular immune
response resulting in a remaining hidden source of
viable fungus on the skin or nail. However, it also
could be due to re-infection from other patients,
fomites, or infective arthrospores found in the
environment23~25.
In concomitant with the treatment study in Raja
Ampat, a study to identify the presence of viable
fungus in the clothing and bedding of the patients
was conducted. The result showed that viable TC
was recovered in 15 out of 40 (37.5%) patients'
clothing samples and 9 out of 40 (22.5%) bedding
samples26. Those results proved that clothing and
bedding are potential fomites for disease trans-
mission and source of re-infection in TI.
The study was followed by an investigation on
the disinfectant activities of several household
cleaners commonly used in Raja Ampat: anionic
detergent 0.2% w/v, sodium hypochlorite solution
5.25% w/v, and a pine oil containing cleaner.
Chlamydospores-rich isolates was subjected to the
cleaner solutions for 15, 30, 60, 120 minutes. It
showed that sodium hypochlorite killed all isolates
within 15 minutes, anionic detergent killed 68%
after 120 minutes, and pine oil containing cleaner
killed 50% after 120 minutes27.
Susceptibility of Trichophyton
concentricum to antifungal agents
Griseofulvin has been the mainstay treatment
Kor J Med Mycol 17(1), 2012
for dermatophytoses in the developing world. It is
relatively cheap and safe for the treatment of
dermatophytoses28. Long term use of antifungal
agent will lead to the emergence of resistant fungus.
In order to elucidate the presence of resistant TC to
antifungal agents, an antifungal susceptibility study
was conducted. Using the disk diffusion method,
40 TC isolates from Raja Ampat population was
subjected to terbinafine, griseofulvin, itraconazole,
and fluconazole. The results showed that the sensi-
tivity was 100% to terbinafine, 65% to griseofulvin,
27.5% to itraconazole, and 2.5% to fluconazole29.
This in vitro result reflected the clinical efficacy of
these antifungals.
Conclusions
Based on the many factors that influence the
chronic-recurrence of TI, a multi-approach program
is needed in TI eradication. Griseofulvin is still
effective, but resistant strains should be given
terbinafine. Since the genetic predisposition is
difficult to eliminate, aside from affordable and
adequate treatment, a susceptible person should be
kept away from infectious source. It is necessary
to identify and to manage the source of re-infection
such as unnoticed nail infection, infected contact
person, fomites, and other potential source of in-
fection in the surrounding environment. Since most
endemic areas are located in remote locations, the
role of local healthcare providers, either profes-
sionals or volunteers are very important to maintain
close monitoring of the patients.
Acknowledgement for the studies in Raja
Ampat
The co-workers were: Drs. S. Widaty, E.
Miranda, D. Anggraini, M. Marissa, J. Chandra, H.
Hutabarat, I.P Bakara, Y. Ilhamsyah, R. Anugerah,
and Mulyati.
-6-
REFERENCES
1. Bonifaz A, Archer-Dubon C, Sal A. Tinea imbricata
or Tokelau. Int J Dermatol 2004;43:506-510
2. Satter EK. Tinea imbricata. Cutis 2009;83:188-191
3. Budimulja U. Dermatophytosis in Indonesia. In
Baxter M (ed.) Proceedings of the VIIIth Congress
of the International Society for Human and Animal
Mycology (ISHAM). New Zealand, Massey Javivers
1982, pp 65-68
4. Rippon JW. Medical mycology, the pathogenic
fungi and the pathogenic actinomycetes, 3rd ed.
Philadelphia: WB Saunders Co; 1988
5. Widyanto, Cases study of tinea imbricata in Mauk,
Tangerang [thesis], Jakarta (Indonesia): University
of Indonesia; 1981
6. Mac Lennan R, O'Keeffe. Superficial fungal in-
fections in an area of low land New Guinea. Aus J
of Dermatol 1966;8:157-163
7. Polunin I. Tinea imbricata in Malaya. Br J Dermatol
1952;64:378-383
8. Halde C, Ong LS. Tinea imbricata treated with
griseofulvin. Am J Trop Med and Hyg 1965;14:1062
-1065
9. Hay RJ, Reid S, Talwat E, Macnamara K. Immune
responses of patients ith tinea imbricata. Br J
Dermatol 1983;108:581-586
10. Budimulja U. Tinea imbricata in central Kalimantan.
Mal J Dermatol 1995;8:17-21
11. Serjeantson S, Lawrence G. Autosomal recessive
inheritance of susceptibility to tinea imbricata. Lancet
1977;309:13-15
12. Ravine D, Turner KJ, Alpern MP. Genetic inheritance
of susceptibility tyo tinea imbricata. J Med Gen 1980;
17:342-348
13. Hay RJ, Reid S, Talwat E, Macnamara K. Endemic
tinea imbricata - a study on Goodenough Island,
Papua New Guinea. Trans R Soc Trop Med Hyg
1984;78:246-251
14. Jablonska S, Blaszcyk M, Kozlowska A. Erythema
 Kusmarinah Bramono: Chronic Recurrent Dermatophytosis in the Tropics: Studies on Tinea Imbricata in Indonesia
gyratum repens-like psoriasis. Int J Dermatol 2000;
39:695-697
15. Cotterman C, Eckert L, Ackerman L. Syphilis
mimicking tinea imbricate and erythema annulare
centrifugum in an immunocompromised patient;
letter to the editor. J Am Acad Dermatol 2009;61:
165-167
16. Batta K, Ramlogan D, Smith AG, Moss C. Tinea
indeciva may mimic the concentric rings of tinea
imbricate. B J Dermatol 2002;147:384
17. Pihet M, Bourgeois H, Maziere JY, Berlioz-Arthaud
A, Bouchara JP, Chabasse D. Isolation of Tricho-
phyton concentricum from chronic cutaneous lesions
in patients from the Solomon islands. Trans R Soc
Trop Med 2008;102:389-393
18. Wingfield AB, Fernandez-Obregon AC, Wignall FS,
Greer D. Treatment of tinea imbricate: a randomized
clinical trial using griseofulvin, terbinafine, itracona-
zole and fluconazole. Br J Dermatol 2004;150:119
-126
19. Makatutu MA, Maskur Z, Manginsengi M,
Sjahruddin B, Nasser M. Ketoconazole in the
treatment of tnea imbricata. Proceedings of the 8th
Regional Conference of Dermatology (Asian-
Australasian), vol.2, Bali, 1988:167-173
20. Budimulja U, Kuswadji, Judonarso J, Widyanto,
Kusanto D, Susilo J, Kartanegara D. Terbinafine in
the treatment of tinea imbricata: an open pilot study.
J Dermatol Treat 1992 (Suppl 1):29-33
21. Budimulja U, Kuswadji, Bramono K, Basuki S,
Judanarso J, Untung LS, et al. A double-blind,
-7-
randomized, stratified controlled study of the
treatment of tinea imbricata with oral terbinafine or
itraconazole. Br J Dermatol 1994;130(Suppl. 43):29
-31
22. Hoque SR, Holden CA. Trichophyton tonsurans in-
fection mimicking tinea imbricate. Clin Exp Dermatol
2007;32:345-346
23. Goksugur N, Karabay O, Kocoglu E. Mycological
flora of the hammams, traditional Turkish bath.
Mycoses 2006;49:411-414
24. Summerbell RC, Krajden S, Kane J. Dermatophytosis
in institution for the elderly. CMAJ 1989;140:112-113
25. Uslu H, Uyanik M, Ayyildiz A. Mycological exami-
nation of the barbers' tools about sources of fungal
infections. Mycoses 2008;51:447-450
26. Marissa M. Isolation of Trichophyton concentricum
from the clothes and sleeping mats of tinea imbricata
patients in Raja Ampat, West Papua [thesis], Jakarta
(Indonesia): University of Indonesia; 2011
27. Hutabarat H. Antifungal activities of disinfectans on
Trichophyton concentricum isolates from Raja Ampat,
West Papua [thesis], Jakarta (Indonesia): University
of Indonesia; 2011
28. Bai Kirubha B. Prescription auditing of griseofulvin
in a tertiary care teaching hospital. Indian J Dermatol
Venereol Leprol 2009;75:588-592
29. Anggraini D. Susceptibility of Trichophyton concen-
tricum isolates from Raja Ampat, West Papua, against
several antifungal agents [thesis], Jakarta (Indonesia):
University of Indonesia; 2011